The inflammatory cytokine Tumor Necrosis Factor (TNF) is an important mediator of the innate immune response to infection. While it is known that TNF is critical to defense against many pathogenic microorganisms, the mechanisms by which TNF mediates this defense are still in need of illumination. The obligate intracellular bacterial pathogen Legionella pneumophila is the causative agent of Legionnaire’s disease and is among the microbes against which TNF is required for optimal defense. Here, we use Legionella as a model pathogen to probe the downstream mechanisms of TNF-mediated defense against intracellular bacterial infection. We find that TNF pre-treatment licenses bone marrow derived macrophages to rapidly engage programmed cell death in response to infection. We additionally find this cell death to be mediated by collective caspase-1, caspase-8, and caspase-11 activity. We demonstrate a requirement for gasdermins in executing this death, indicating pyroptosis. Furthermore, we are able to demonstrate TNF-licensed restriction of Legionella replication mediated by caspases-1, -8, and -11 in parallel. We then show that caspase-8 activity restricts Legionella replication in vivo. We follow up these studies with investigation of additional TNF-mediated protective mechanisms, and present data which suggest a role for the protein IRG1 in TNF-mediated restriction of Legionella replication, as well as data which indicate suboptimal cytokine production of TNF-deficient cells in the lung during Legionella infection. Overall, we thoroughly dissect and define the mechanistic role of TNF in strict limitation of Legionella infection and present new evidence of parallelism between caspases when mediating pyroptosis in response to infection with intracellular L. pneumophila.